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Intracortical origin of visual maps

Abstract

Previous experiments indicate that the shape of maps of preferred orientation in the primary visual cortex does not depend on visual experience. We propose a network model that demonstrates that the orientation and direction selectivity of individual units and the structure of the corresponding angle maps could emerge from local recurrent connections. Our model reproduces the structure of preferred orientation and direction maps, and explains the origin of their interrelationship. The model also provides an explanation for the correlation between position shifts of receptive fields and changes of preferred orientations of single neurons across the surface of the cortex.

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Figure 1: Connection strengths and activity states.
Figure 2: Formation of PO maps.
Figure 3: Formation of PD maps. Direction preference of the cortical columns shown in Fig. 2, obtained in the same computer simulation.
Figure 4: Geometry of receptive fields.
Figure 5: Analysis of the activity dynamics.

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References

  1. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).

    Article  CAS  Google Scholar 

  2. Blasdel, G. G. & Salama, G. Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579–585 (1986).

    Article  CAS  Google Scholar 

  3. Grinvald, A. et al. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324, 351–354 (1986).

    Article  Google Scholar 

  4. von der Malsburg, C. Self-organization of orientation selective cells in the striate cortex. Kybernetik 14, 85–100 (1973).

    Article  CAS  Google Scholar 

  5. Swindale, N. V. A model for the formation of orientation columns. Proc. R. Soc. Lond. B Biol. Sci. 215, 211–230 (1982).

    Article  CAS  Google Scholar 

  6. Obermayer, K., Ritter, H. & Schulten, K. A principle for the formation of the spatial structure of cortical feature maps. Proc. Natl. Acad. Sci. USA 87, 8345–8349 (1990).

    Article  CAS  Google Scholar 

  7. Miller, K. D. A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between on- and off-center inputs. J. Neurosci. 14, 409–441 (1994).

    Article  CAS  Google Scholar 

  8. Wolf, F. & Geisel, T. Spontaneous pinwheel annihilation during visual development. Nature 395, 73–78 (1998).

    Article  CAS  Google Scholar 

  9. Goedecke, I., Kim, D.-S., Bonhoeffer, T. & Singer, W. Development of identical maps for two eyes without common visual experience. Eur. J. Neurosci. 9, 1754–1762 (1997).

    Article  Google Scholar 

  10. Goedecke, I. & Bonhoeffer, T. Development of identical orientation maps for two eyes without common visual experience. Nature 379, 251–254 (1996).

    Article  CAS  Google Scholar 

  11. Crair, M. C., Gillespie, D. C. & Stryker, M. P. The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–570 (1998).

    Article  CAS  Google Scholar 

  12. Ben-Yishai, R., Bar-Or, R. & Sompolinsky, H. Theory of orientational tuning in visual cortex. Proc. Natl. Acad. Sci. USA 92, 3844–3848 (1995).

    Article  CAS  Google Scholar 

  13. Somers, D. C., Nelson, S. B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448–5465 (1995).

    Article  CAS  Google Scholar 

  14. Sompolinsky, H. & Shapley, R. New perspectives on the mechanisms for orientation selectivity. Curr. Opin. Neurobiol. 7, 514–522 (1997).

    Article  CAS  Google Scholar 

  15. McLaughlin, D., Shapley, R., Shelley, M. & Wielaard, D. J. A neuronal network model of macaque primary visual cortex (V1): orientation selectivity and dynamics in the input layer 4Calpha. Proc. Natl. Acad. Sci. USA 97, 8087–8092 (2000).

    Article  CAS  Google Scholar 

  16. Ahmed, B., Anderson, J., Douglas, R., Martin, K. & Nelson, J. Polyneural innervation of spiny stellate neurons in cat visual cortex. J. Comp. Neurol. 341, 39–49 (1994).

    Article  CAS  Google Scholar 

  17. Amari, S. Dynamics of pattern formation in lateral-inhibition type neural fields. Biol. Cybern. 27, 77–87 (1977).

    Article  CAS  Google Scholar 

  18. Tsodyks, M. V. & Sejnowski, T. J. Associative memory and hippocampal place cells. Int. J. Neural Sys. 6, 81–86 (1995).

    Google Scholar 

  19. Bonhoeffer, T. & Grinvald, A. Orientation columns in cat are organized in pin-wheel like patterns. Nature 353, 429–431 (1991).

    Article  CAS  Google Scholar 

  20. Obermayer, K. & Blasdel, G. Geometry of orientation and ocular dominance columns in monkey striate cortex. J. Neurosci. 13, 4114–4129 (1993).

    Article  CAS  Google Scholar 

  21. Swindale, N. V., Matsubara, J. A. & Cynader, M. S. Surface organization of orientation and direction selectivity in cat area 18. J. Neurosci . 16, 6945–6964 (1996).

    Article  Google Scholar 

  22. Shmuel, A. & Grinvald, A. Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J. Neurosci. 16, 6945–6964 (1996).

    Article  CAS  Google Scholar 

  23. Das, A. & Gilbert, C. Distortions of visuotopic map match orientation singularities in primary visual cortex. Nature 387, 594–598 (1997).

    Article  CAS  Google Scholar 

  24. Ernst, U., Pawelzik, K., Tsodyks, M. & Sejnowski, T. Relation between retinotopical and orientation maps in visual cortex. Neural Comput. 11, 375–379 (1999).

    Article  CAS  Google Scholar 

  25. Maffei, L. & Galli-Resta, L. Correlation in the discharges of neighboring rat retinal ganglion cells during prenatal life. Proc. Natl. Acad. Sci. USA 87, 2861–2864 (1990).

    Article  CAS  Google Scholar 

  26. Gilbert, C. & Wiesel, T. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J. Neurosci. 9, 2432–2442 (1989).

    Article  CAS  Google Scholar 

  27. Loewel, S. & Singer, W. Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255, 209–212 (1992).

    Article  Google Scholar 

  28. Malach, R., Amir, Y., Harel, M. & Grinvald, A. Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proc. Natl. Acad. Sci. USA 90, 10469–10473 (1993).

    Article  CAS  Google Scholar 

  29. Reid, R. C. & Alonso, J. M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).

    Article  CAS  Google Scholar 

  30. Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252 (1996).

    Article  CAS  Google Scholar 

  31. Loewel, S. et al. The layout of orientation and ocular dominance domains in area 17 of strabismic cats. Eur. J. Neurosci. 10, 2629–2643 (1998).

    Article  Google Scholar 

  32. Rojer, A. S. & Schwartz, E. L. Cat and monkey cortical columnar patterns modelled by bandpass-filtered 2D white noise. Biol. Cybern. 62, 381–391 (1990).

    Article  CAS  Google Scholar 

  33. Shouval, H. Z, Goldberg, D. H, Jones, J. P, Beckerman, M. & Cooper, L. N. Structured long-range connections can provide a scaffold for orientation maps. J. Neurosci. 20, 1119–1128 (2000).

    Article  CAS  Google Scholar 

  34. Wilson, H. & Cowan, J. A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Biol. Cybern. 13, 55–80 (1973).

    CAS  Google Scholar 

  35. Grossberg, S. Nonlinear neural networks: principles, mechanisms, and architectures. Neural Net. 1, 17–61 (1988).

    Article  Google Scholar 

  36. Wolf, F., Bauer, H.-U., Pawelzik, K. & Geisel, T. Organization of the visual cortex. Nature 382, 306–307 (1996).

    Article  CAS  Google Scholar 

  37. Tsodyks, M., Kenet, T, Arieli, A. & Grinvald, A. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286, 1943–1946 (1999).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank S. Hoshtein, A. Shmuel, S. Loewel, W. Singer and F. Wolf for comments on an earlier draft of the manuscript. This work was supported by grants from Max-Planck-Gesellschaft, Deutsche Forschungsgemeinschaft, Office of Naval Research, Minerva Foundation and the Hanse Wissenschaftskolleg.

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Correspondence to M. V. Tsodyks.

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Ernst, U., Pawelzik, K., Sahar-Pikielny, C. et al. Intracortical origin of visual maps. Nat Neurosci 4, 431–436 (2001). https://doi.org/10.1038/86089

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